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Population Genetics of Raccoons in the Eastern United States With Implications for Rabies Transmission and Spread

Dissertation
Author: Serena Ann Reeder Carroll
Abstract:
A central research question in disease ecology concerns how a pathogen moves throughout space and time (Anderson and May 1978). For directly transmitted zoonoses, this process is likely influenced by the biological and environmental characteristics of both the pathogen and its host (Real and McElhany 1996; Hess et al. 2001; Real and Biek 2007). Although these interactions are complex, one can attempt to discern the relative contribution of each component by testing explicit hypotheses systematically. The motivation for this research was to increase our understanding of how a directly transmitted pathogen spreads in a wildlife population, and specifically, to examine host factors that might influence pathogen transmission or spread. In this dissertation, the raccoon rabies model system was used to explore how social structure and landscape heterogeneity influence pathogen transmission. We used genetic data to generate relatedness estimates of raccoons and tested whether social organization influenced host contact rates or raccoon rabies transmission (Chapter 2). Additionally, we used genetic data to define the historical and contemporary population structure of raccoons throughout the range of the raccoon rabies virus variant (RRV). This information was used to determine whether landscape heterogeneity in the form of historically defined suture-zones (Remington 1968) in the eastern US resulted in limited raccoon dispersal or barriers to gene flow that might also have affected the spread of RRV (Chapter 3). Finally, surveillance data and modeling techniques were used to examine the influence of host biology (home range, incubation, and infectious periods) on the spatial and temporal clustering or aggregation of raccoon rabies in a multi-host system, raccoons and skunks, in the northeastern US (Chapter 4). Each of the chapters discusses the specific hypotheses tested and results in depth, and a summary can be found in Chapter 5.

Table of Contents

Chapter 1. Introduction 1 1.1 Background 1 1.2 Goals of the Dissertation 4 1.3 Raccoons and Rabies as a Model System 4 1.4 Population Genetics of Raccoons (Procyon lotor) Corresponding to a New Focus of Raccoon Rabies in Northeastern Ohio: Implications for Transmission 12 1.5 Historical and Contemporary Evolution Account for Population Subdivision in Raccoon (Procyon lotor) Populations in the Eastern United States 13 1.6 Spatiotemporal Interactions Of Enzootic Raccoon Rabies 14

Chapter 2. Population Genetics of Raccoons (Procyon lotor) Corresponding to a New Focus of Raccoon Rabies in Northeastern Ohio: Implications for Transmission 16 2.1 Introduction 16 2.2 Materials and Methods 21 2.2.1 Raccoon Samples and Collection Localities 21 2.2.2 DNA Isolation and Microsatellites 23 2.2.3 Mitochondrial DNA 25 2.2.4 Population Genetic Structure 26

2.2.5 Sex Ratio and Haplotype Distribution 27 2.2.6 Relatedness 28 2.3 Results 28 2.3.1 Microsatellites 28 2.3.2 Population Genetic Structure 29 2.3.3 Mitochondrial DNA 33 2.3.4 Rabid Versus Non-Rabid Raccoons 36 2.3.5 Relatedness 36 2.4 Discussion 39

Chapter 3. Historical and Contemporary Evolution Account for Population Subdivision in Raccoon (Procyon lotor) Populations in the Eastern United States 44 3.1 Introduction 44 3.1.1 Landscape Genetics and Relevance to Raccoon Rabies 44 3.1.2 Suture-Zones As Historic or Contemporary Barriers to Gene Flow? 46 3.1.3 A Common Phylogeographic Boundary for the Southeastern United States Eco-Region? 51 3.2 Materials and Methods 53 3.2.1 Raccoon Samples 53 3.2.2 DNA Isolation and Microsatellites 55 3.2.3 Population Genetic Structure 56

3.2.4 Mitochondrial DNA 57 3.2.5 Tests of Selective Neutrality 58 3.3 Results 59 3.3.1 Microsatellites 59 3.3.2 Population Genetic Structure 60 3.3.3 Mitochondrial DNA 63 3.3.4 Tests of Selective Neutrality 65 3.4 Discussion 66 3.4.1 Contemporary Population Structure and Barriers to Gene Flow 66 3.4.2 Historical Population Structure and Barriers to Gene Flow 68 3.4.3 Implications for a Southeastern US Eco-Region 69 3.4.4 Factors Influencing Raccoon Rabies Spread During the 1950s-1970s 70

Chapter 4. Spatiotemporal Interactions Of Enzootic Raccoon Rabies 73 4.1 Introduction 73 4.2 Materials and Methods 77 4.3 Results 82 4.4 Discussion 85

Chapter 5. Summary and Conclusions 89

References/Bibliography 93

List of Figures

Figure 1.1 Range map of raccoons in North America 5 Figure 1.2 Distribution of major terrestrial reservoirs of rabies in the United States and Puerto Rico 7 Figure 2.1 Map of collection localities of 182 raccoons sampled in northeastern Ohio 22 Figure 2.2 Allocation of raccoons into 2 populations, as suggested by the Structure analysis 31 Figure 2.3 Number of populations in northeastern Ohio identified by Geneland 32 Figure 2.4 Minimum spanning network of mitochondrial haplotypes found in northeastern Ohio 35 Figure 2.5 Geographic distance vs. average relatedness for (a) all raccoons, and (b) female-female, female-male, and male-male dyads 37 Figure 3.1 Digital version of Remington’s suture-zones (1968) 47 Figure 3.2 Location of the Suwannee River Watershed 50 Figure 3.3 Sampling localities of 625 raccoons throughout the Eastern US 54 Figure 3.4 Number of raccoon populations in the Eastern US identified by Geneland 60 Figure 3.5 Distribution of the 3 haplotype groups 64 Figure 4.1 Massachusetts county map, showing Barnstable County 79

Figure 4.2 Raccoon rabies in Massachusetts, 2000-2005 80 Figure 4.3 Spatial clustering of raccoon rabies virus in raccoons (a) and skunks (b) 82/83 Figure 4.4 Spatial-temporal interaction of raccoons infected with raccoon rabies at a critical distance of 6 kilometers and 8 weeks 84 Figure 4.5 Spatial-temporal interaction of skunks infected with raccoon rabies at a critical distance of 6 kilometers and 8 weeks 85

List of Tables Table 2.1 Primers used for amplification of 7 previously described microsatellite loci 24 Table 2.2 Microsatellite allelic diversity for all 7 loci 29 Table 2.3 Number of populations (K) estimated using Structure 30 Table 2.4 Definition of 16 unique mitochondrial haplotypes found in 182 raccoons in northeastern Ohio. Polymorphic sites contributing to haplotype definitions are shown 33 Table 2.5 Relatedness calculations and 95% confidence intervals for rabid and non-rabid raccoons overall as well as rabid and non-rabid raccoons by sex 39 Table 3.1 Allelic diversity and size range for all 7 loci 59 Table 3.2 Number of populations (K) estimated using Structure 61 Table 3.3 Population pairwise F ST and φ ST values 62 Table 3.4 Haplotype and nucleotide diversity indices and neutrality tests 65 Table 4.1 Number of captures recorded between 2000-2005 in Massachusetts 79

1 CHAPTER 1 Introduction

1.1 BACKGROUND In 1978, Anderson and May proposed that the host-parasite relationship involved more than just a parasite’s impact on its host. Rather, the complex interactions between the two entities influenced the rate of parasite transmission among hosts, with multiple factors leading to unique patterns of parasite (or pathogen) spread. Relevant factors include host behavior, social or genetic population structure, population density or abundance, contact rate, parasite/pathogen virulence, transmission efficiency, and latency period, among others (Schauber et al. 2007; Barton et al. 2010). Of those, population structure is especially interesting in that host population structure can influence pathogen virulence (Boots et al. 2004) and the spread of infectious disease, yet pathogens can similarly influence host genetic variation (Kellam and Weiss 2006). Furthermore, pathogens and parasites may act as moderators of population structure (Chapman et al. 2005), illustrating the fact that host-parasite interactions are often bidirectional. To complicate the relationship between pathogens and hosts, conflicts between rapidly evolving pathogens and slowly evolving hosts can act to accelerate changes in host behavior and thus create new niches for emerging pathogens (Morens et al. 2004). Local adaptation of pathogens to particular host genotypes can occur and may result in the formation of population structure in the pathogen. This structure can lead to different infectivities in vector populations and subsequently modify the patterns of disease transmission and spread (Joy et al. 2008).

2 The reality that parasites and their hosts not only interact within populations but also among them (i.e., metapopulation structure) further complicates the question of how parasites move though space and time. Here, at least two levels of host-parasite population dynamics must be taken into account when reconstructing transmission events. Indeed, 30 years later, the question of how parasites/pathogens move throughout space and time remains central to disease ecology (Hudson et al. 2001; Real and Biek 2007). While elements borrowed from predator-prey models have been combined with elements from conventional epidemiology (Anderson and May 1980) to model infectious disease dynamics and transmission, typical predator-prey models assume that predators and prey are similar entities in terms of their life history characteristics and population size. While this is certainly the case for a multitude of systems, infectious disease is an exception (Vandermeer and Goldberg 2003). In this case, the predators are pathogens (viruses, bacteria, or other microorganisms) and are generally small with short generation times and rapid dynamics whereas the prey (hosts) are much larger and have relatively slow dynamics and longer generation times in comparison (Anderson and May 1991; Vandermeer and Goldberg 2003). In the context of classical epidemiology, SIR (susceptible-infected-recovered) models assume that hosts are homogeneously mixed and pathogen transmission is usually examined against a background of constant hosts (Anderson and May 1980; Vandermeer and Goldberg 2003). One problem with this methodology is that hosts are unlikely to be uniform in their distribution (Anderson and May 1991; Vandermeer and Goldberg 2003), and undetected population structure can

3 produce potentially misleading results (Marchini et al. 2004). Differences both within and among populations of parasites and hosts can create heterogeneity. Heterogeneity can be problematic on a variety of levels because of the different forms that it can take. Not only can hosts or parasites be heterogeneous (genetically, spatially, etc.), but the landscape upon which these processes are occurring can also take a heterogeneous form (Real and Biek 2007). A new field, landscape genetics, combines landscape ecology and population genetics approaches to determine the influence of landscape features on microevolutionary processes (Sork et al. 1999; Manel et al. 2003). While the field has been formally recognized only in recent years, scientists have recognized the importance of landscape features on the distribution of organisms for centuries. During the early 1800s, the botanist Augustin Pyramus de Candolle wrote that organism distributions varied across the landscape and depended on physical causes operating on different time scales. Not long afterwards, Alfred Russel Wallace, sometimes referred to as the father of biogeography, described a boundary separating fauna in the Australian Region from the Oriental Region in the Malay Archipelago (the Wallace line) in the 1850s (Manel et al. 2003). Overlaying genetic differences onto the landscape to detect barriers to gene flow looks to be a promising technique for understanding how these heterogeneities are manifested. As Sork et al. (1999) recently stated: “Regardless of whether landscape heterogeneity is natural or created by recent anthropogenic disturbance, a critical question that researchers can now address is the extent to which the landscape context of populations influences gene movement.” These techniques have already been used to describe landscape features that act as barriers to gene flow in a variety of host species

4 with associated pathogens, especially with the goal of informing disease mitigation and management strategies (Blanchong et al. 2008; DeYoung et al. 2009; Root et al. 2009; Barton et al. 2010).

1.2 GOALS OF THE DISSERTATION This dissertation represents a body of work aimed at elucidating the factors involved in the transmission and spread of a zoonotic disease in a wildlife population. Specifically, three host-based approaches are taken to gain insight into how raccoon rabies has spread throughout the eastern seaboard. The first examines raccoon relatedness estimates to infer the impact of social structure on disease transmission. The second method uses raccoon population genetics to identify historical and contemporary barriers to gene flow and how that might influence rabies spread. The final method uses surveillance data and modeling techniques to examine the spatiotemporal relationship of raccoon rabies virus in two wildlife species, the raccoon and the skunk, to determine the relative influence of host home range, incubation period, and infectious period on the spatial and temporal clustering or aggregation of raccoon rabies in a multi-host system. After an introduction into raccoons and rabies and their utility as a model system, each of these approaches will be summarized below.

1.3 RACCOONS AND RABIES AS A MODEL SYSTEM The common raccoon (Procyon lotor) is a mesocarnivore distributed throughout North America (Figure 1.1), with few exceptions, from Canada to Panama in Central America (Hall and Kelson 1959; Lotze and Anderson 1979; Wilson and Ruff 1999;

5 Zeveloff 2002). The earliest known Procyon fossil uncovered in North America dates to the Pliocene (Simpson 1945; Lotze and Anderson 1979), approximately 5.5 to 2 million years before the present, indicating the raccoon’s long association with the New World. As generalists, they are easily adaptable and can thrive in many diverse habitats, often resulting in high density populations in urban and suburban environments. Their adaptability is further illustrated by their successful introduction to France, Germany, the former Soviet Union, and many Caribbean islands (Zeveloff 2002).

Figure 1.1 Range map of raccoons in North America (Wilson and Ruff 1999)

Traditionally, raccoons have been regarded as solitary animals except during times of high resource availability (Gehrt and Fritzell 1998; Zeveloff 2002); however, recent studies have found that raccoons may be more social than previously thought and

6 small, non-aggressive groups of 3-4 males may form (Gehrt and Fritzell 1998). Raccoons are highly vagile, and home range estimates vary greatly depending on the habitat (Zeveloff 2002). Raccoons typically occupy smaller home ranges when densities are high, or in urban/suburban areas where food and water resources are concentrated and are readily available (Zeveloff 2002; Prange et al. 2004). Dispersal is predominantly male biased as females are philopatric (Ratnayeke et al. 2002). Raccoons are hosts to a number of zoonotic diseases including rabies, an acute, progressive encephalitis transmitted primarily via the bite of a rabid animal. Rabies is a nonsegmented, negative-strand RNA virus in the family Rhabdoviridiae, genus Lyssavirus (Lyles and Rupprecht 2006). Worldwide, rabies remains a significant cause of mortality and accounts for more than 55,000 human deaths each year (World Health Organization 2008). With the elimination of enzootic dog rabies in the United States (US), rabies remains a significant problem primarily in wildlife populations (Velasco- Villa et al. 2008; Blanton et al. 2009). Distinct rabies virus variants (Figure 1.2) have been associated with raccoons, skunks, foxes, coyotes, mongooses, and bats in the US (Rupprecht et al. 1987; Blanton et al. 2009). The raccoon rabies virus (RRV) variant, which occurs throughout the eastern United States, is of particular public health concern due to frequent human/raccoon interactions. The first documented human fatality due to RRV occurred in Virginia in 2003 (Silverstein et al. 2003). Despite the long evolutionary history of raccoons in the New World, raccoon rabies is a relatively recent development. The first rabid raccoon in the United States was identified in California in 1936 (McLean 1975). After that time, raccoon rabies was reported rather infrequently and was attributed to spillover events

7 from other rabies virus hosts. In 1947, a rabid raccoon was identified in Brevard County in central Florida (Kappus et al. 1970; Bigler et al. 1973). Rabies in raccoons spread within Florida during the 1950s and throughout Georgia, Alabama, and South Carolina over the next 20 years (Held et al. 1967; Kappus et al. 1970; McLean 1971; Bigler et al. 1973; Niezgoda et al. 2002).

Figure 1.2 Distribution of major terrestrial reservoirs of rabies in the United States and Puerto Rico (Blanton et al. 2009).

During the late 1970s, rabies in raccoons was detected in the Mid-Atlantic States along the border of Virginia and West Virginia in Pendleton County, West Virginia (Nettles et al. 1979; Jenkins and Winkler 1987; Rupprecht and Smith 1994). Antigenic

8 analysis demonstrated its relatedness to southern cases and indicated that this outbreak was likely the result of long distance translocations of raccoons for hunting purposes (Nettles et al. 1979; Smith et al. 1984). Translocations of raccoons were common practice during this time with over 3,500 raccoons transported from Florida to Virginia between 1977 and 1981 (Jenkins et al. 1988; Rupprecht and Smith 1994). This sparked one of the largest rabies epizootics in history as the outbreak spread both north and south from West Virginia. During the 1980’s, raccoon rabies continued to spread. It arrived in Maryland as early as 1981 and reached Pennsylvania and the District of Columbia by 1982. Delaware first reported rabid raccoons in 1987, and New Jersey followed in 1988. Raccoon rabies reached the western townships of Connecticut (near New York) in 1991 and spread across the state in just 5 years. In 1994/1995, the southeastern epizootic and Mid- Atlantic epizootic foci met in North Carolina and by 1999, the raccoon rabies front reached Canada. Today, raccoon rabies can be found along the eastern seaboard from Florida to Maine, with the western edge occurring along the Ohio/Pennsylvania border in the northern part of its range, extending into eastern Tennessee and south to Alabama (Blanton et al. 2009; see also Figure 1.2). RRV appears to have since been eliminated from Ontario, Canada, with the last reported case occurring in 2005 (Rosatte et al. 2009). Over 50,000 rabid raccoons have been diagnosed to date. The southeastern and Mid-Atlantic epizootics differed in certain spatial and temporal aspects (Childs et al. 2001). For example, the southern states experienced smaller, less frequent epizootics, without a clear temporal dynamic. The northern epizootics seemed to be larger and more frequent. This is possibly due to the high human

9 population density from Virginia to Massachusetts, or perhaps, to more favorable habitats for raccoons in the north. Extremely high raccoon densities have been found in urban parks and suburban areas (Riley et al. 1998), indicating a positive association with human population density (Childs et al. 2001). The resulting increased raccoon density could have then contributed to larger rabies epizootics (Childs et al. 2001). The restriction of RRV to the eastern US is likely due to a combination of natural geographic barriers and barriers created by vaccination. Physical barriers, such as mountains, large rivers, and major highways may restrict or slow raccoon movement or dispersal (Lucey et al. 2002; Smith et al. 2005; Biek et al. 2007; Cullingham et al. 2009). Alternatively, these areas may sustain lower raccoon population densities, resulting in lower contact rates among infected individuals and slower RRV spread. Additionally, oral rabies vaccination (ORV) has been implemented for enhanced restriction of newly infected areas (Smith et al. 2002; Rupprecht et al. 2004; Slate et al. 2005). The ORV campaign involves the vaccination of raccoons against rabies via aerial and ground distribution of fishmeal polymer or coated sachet baits containing a vaccinia-rabies glycoprotein (V-RG) recombinant virus (Wiktor et al. 1984; Rupprecht et al. 1986; Hanlon et al. 1998; Rupprecht et al. 2004; Slate et al. 2005). Effectively, a barrier of vaccinated raccoons is established thus diminishing the pool of susceptible animals and limiting the ability of the rabies virus to spread. The first release of the ORV bait was in 1990 on Parramore Island, Virginia (Hanlon et al. 1998). New York began baiting in 1995 and by 2001, states participating in the ORV campaign included Florida, Maryland, Massachusetts, New Hampshire, New York, Ohio, and Virginia. Sixteen states currently distribute oral rabies vaccines for

10 raccoons (http://www.aphis.usda.gov/wildlife_damage/oral_rabies/ ). As discussed above, this strategy, in combination with the use of natural physical barriers to raccoons, has helped to curb the westward spread of RRV; however, long distance translocations may still pose a significant threat (Rupprecht et al. 2004; Slate et al. 2009). An added concern for controlling the spread of RRV is the potential involvement of skunks in maintaining and/or transmitting the virus in the northeastern US. While RRV is primarily maintained and transmitted by raccoons, skunks can be infected with RRV and have been shown to be important secondary hosts (Guerra et al. 2003). Independent skunk-to-skunk transmission of RRV has not yet been identified, but previous studies (Guerra et al. 2003) have noted that rabies epizootics in raccoons and skunks are closely coupled. Although skunks may consume ORV baits, this method has not proven efficient in preventing rabies in skunks either due to the vaccine itself or to poor vaccine delivery, whereby the vaccine is lost to the environment as the skunks puncture the vaccine sachets (Charlton et al. 1992; Guerra et al. 2003; Grosenbaugh et al. 2007; United States Department of Agriculture 2007). Host-switching or host-shift events are also important considerations for RRV control. Recently, Streicker et al. (2010) presented evidence of cross species transmission (CST) of bat rabies viruses and demonstrated that the probability of CST and host shift decreased with increasing phylogenetic distance of host species. The phylogenetic similarity of host species, and to a lesser extent, the geographic overlap between species, played more important roles in predicting CST than did similarity of host ecological traits (Streicker et al. 2010). This has important implications for host shifts involving RRV. Mutation in RRV could result in a variant that readily crosses over

11 into another host, such as the skunk or another mesocarnivore, and becomes sustained after traversing a flattened fitness valley and adapting to its new host (Streicker et al. 2010). Although this was not previously thought to be common with rabies, potential raccoon to raccoon transmission may have occurred after infection with a fox strain in New York in the late 1940’s (McLean 1975; Winkler and Jenkins 1991). Furthermore, recent transmission of a bat rabies virus variant from bats to skunks and foxes in Arizona with sustained carnivore to carnivore transmission highlights the very real possibility of crossing over and adaptation to a new species, even when the phylogenetic distance between host species is great (Leslie et al. 2006; http://www.avma.org/onlnews/javma/nov09/091115m.asp ). The origin of raccoon rabies is somewhat of a mystery (Rupprecht and Smith 1994). The variant is highly adapted to raccoons, and sequence identity of RRVs in raccoons from Florida to Maine is on the order of 99%. In terms of phylogenetics, RRV isolates clearly form a monophyletic clade. It appears that their closest relative is the South Central Skunk variant (Rupprecht and Smith 1994; Smith et al. 1995); however, Szanto et al. (2008) recently suggested that RRV emerged from a North American bat rabies virus variant, either directly or via adaptation of the South Central Skunk variant. Bat-associated origins for RRV have been suggested previously, and three types of transmission from bats to raccoons have been hypothesized: bat bites to the raccoon, aerosol transmission, and consumption of bats as food by raccoons (Winkler and Jenkins 1991). One line of evidence in support of this idea concerns a rabid raccoon trapped in the vicinity of a bat cave in Texas. The raccoon in question was infected with a rabies virus similar to that of a Mexican freetail bat (Tadarida brasiliensis) isolate (Constantine

12 1962; Winkler and Jenkins 1991). In a later study in Florida, however, no evidence was found for bat to raccoon transmission.

1.4 POPULATION GENETICS OF RACCOONS (PROCYON LOTOR) CORRESPONDING TO A NEW FOCUS OF RACCOON RABIES IN NORTHEASTERN OHIO: IMPLICATIONS FOR TRANSMISSION

The integration of population genetic and epidemiologic data has the power to provide novel insight into patterns of pathogen transmission within host populations. Recently, these techniques have been used to suggest that relatedness and social structure might play a role in influencing contact rates and disease transmission in a variety of systems (Root et al. 2004; Blanchong et al. 2007). In this study, we test the hypothesis that social structure, inferred through relatedness estimates, influences disease transmission using RRV as a model system. Female raccoons are philopatric and live in related groups with shared home ranges (Gehrt and Fritzell 1998; Ratnayeke et al. 2002). This social structure implies that females contact other relatives more frequently than non-related individuals. If rabies is spread primarily due to female philopatry, then there should be a sex bias, and rabid raccoons should be more highly related. On the other hand, dispersal is predominantly male biased in this system (Gehrt and Fritzell 1998; Zeveloff 2002). If rabies is spread by highly dispersive, unrelated males then relatedness estimates of rabid males should be lower than expected. Alternatively, raccoon genetic/social structure may not strongly

13 influence RRV transmission, in which case relatedness estimates should not significantly deviate from zero.

1.5 HISTORICAL AND CONTEMPORARY EVOLUTION ACCOUNT FOR POPULATION SUBDIVISION IN RACCOON (PROCYON LOTOR) POPULATIONS IN THE EASTERN UNITED STATES

Landscape genetics, a newly emerging field combining molecular population genetics and landscape ecology, can be used to understand how heterogeneity across the landscape affects population structuring at different geographic and temporal scales (Sork et al. 1999; Manel et al. 2003). Since rabies is a directly transmitted pathogen requiring animal to animal contact for transmission, it is reasonable to assume that landscape factors that act as obstacles to raccoon movement will also act as barriers to RRV progression (Real and Biek 2007; Cullingham et al. 2008; Cullingham et al. 2009). The purpose of this study is to test the hypothesis that the Northeastern-Central and Northern Florida Suture-Zones, areas of geographic overlap between major biotic assemblages with the potential for hybridization, (Remington 1968; Swenson and Howard 2004) have acted as geographic barriers to gene flow in raccoons and their associated pathogen, RRV. Although these areas are presumed to represent historical barriers, it is unclear whether they constitute contemporary barriers or if secondary contact has resulted in gene flow and/or population mixing. By examining a combination of nuclear and mitochondrial markers, we can distinguish between potential historical and contemporary

Full document contains 126 pages
Abstract: A central research question in disease ecology concerns how a pathogen moves throughout space and time (Anderson and May 1978). For directly transmitted zoonoses, this process is likely influenced by the biological and environmental characteristics of both the pathogen and its host (Real and McElhany 1996; Hess et al. 2001; Real and Biek 2007). Although these interactions are complex, one can attempt to discern the relative contribution of each component by testing explicit hypotheses systematically. The motivation for this research was to increase our understanding of how a directly transmitted pathogen spreads in a wildlife population, and specifically, to examine host factors that might influence pathogen transmission or spread. In this dissertation, the raccoon rabies model system was used to explore how social structure and landscape heterogeneity influence pathogen transmission. We used genetic data to generate relatedness estimates of raccoons and tested whether social organization influenced host contact rates or raccoon rabies transmission (Chapter 2). Additionally, we used genetic data to define the historical and contemporary population structure of raccoons throughout the range of the raccoon rabies virus variant (RRV). This information was used to determine whether landscape heterogeneity in the form of historically defined suture-zones (Remington 1968) in the eastern US resulted in limited raccoon dispersal or barriers to gene flow that might also have affected the spread of RRV (Chapter 3). Finally, surveillance data and modeling techniques were used to examine the influence of host biology (home range, incubation, and infectious periods) on the spatial and temporal clustering or aggregation of raccoon rabies in a multi-host system, raccoons and skunks, in the northeastern US (Chapter 4). Each of the chapters discusses the specific hypotheses tested and results in depth, and a summary can be found in Chapter 5.